Right on target: eradicating leukemic stem cells

Trends in Molecular Medicine

Volumn 13, Issue 11, 2007, Pages 470-481

  Krause, Daniela S ^a   Van Etten, Richard A ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b TUFTS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE GRANULOCYTIC LEUKEMIA; LEUKEMIA CELL; RECURRENT DISEASE; REVIEW; SIGNAL TRANSDUCTION; STEM CELL;

ACUTE DISEASE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; HUMANS; LEUKEMIA; LEUKEMIA, MYELOID; MICE; MODELS, BIOLOGICAL; NEOPLASTIC STEM CELLS;

MUS;

EID: 36048985371     PISSN: 14714914     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molmed.2007.09.003     Document Type: Review

References (99)

1. Bruce W.R., and Van Der Gaag H. A quantitative assay for the number of murine lymphoma cells capable of proliferation in vivo. Nature 199 (1963) 79-80
2. Lapidot T., et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367 (1994) 645-648
3. Reya T., et al. Stem cells, cancer, and cancer stem cells. Nature 414 (2001) 105-111
4. Pardal R., et al. Applying the principles of stem-cell biology to cancer. Nat. Rev. Cancer 3 (2003) 895-902
5. Passegue E., et al. Normal and leukemic hematopoiesis: are leukemias a stem cell disorder or a reacquisition of stem cell characteristics?. Proc. Natl. Acad. Sci. U. S. A. 100 Suppl. 1 (2003) 11842-11849
6. Castor A., et al. Distinct patterns of hematopoietic stem cell involvement in acute lymphoblastic leukemia. Nat. Med. 11 (2005) 630-637
7. Matsui W., et al. Characterization of clonogenic multiple myeloma cells. Blood 103 (2004) 2332-2336
8. Al-Hajj M., et al. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 3983-3988
9. Singh S.K., et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 63 (2003) 5821-5828
10. O'Brien C.A., et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445 (2007) 106-110
11. Li C., et al. Identification of pancreatic cancer stem cells. Cancer Res. 67 (2007) 1030-1037
12. Appelbaum F.R., et al. Acute myeloid leukemia. Hematology Am. Soc. Hematol. Educ. Program. (2001) 62-86
13. Hughes T.P., et al. Frequency of major molecular responses to imatinib or interferon alfa plus cytarabine in newly diagnosed chronic myeloid leukemia. N. Engl. J. Med. 349 (2003) 1423-1432
14. Cortes J., et al. Discontinuation of imatinib therapy after achieving a molecular response. Blood 104 (2004) 2204-2205
15. van Rhenen A., et al. The novel AML stem cell associated antigen CLL-1 aids in discrimination between normal and leukemic stem cells. Blood 110 (2007) 2659-2666
16. Yilmaz O.H., et al. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 441 (2006) 475-482
17. Krivtsov A.V., et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 442 (2006) 818-822
18. Krause D.S., et al. Requirement for CD44 in homing and engraftment of BCR-ABL-expressing leukemic stem cells. Nat. Med. 12 (2006) 1175-1180
19. Jin L., et al. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat. Med. 12 (2006) 1167-1174
20. Bonnet D., and Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3 (1997) 730-737
21. Hope K.J., et al. Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nat. Immunol. 5 (2004) 738-743
22. Morrison S.J., and Weissman I.L. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1 (1994) 661-673
23. Baum C.M., et al. Isolation of a candidate human hematopoietic stem-cell population. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 2804-2808
24. Blair A., et al. Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo. Blood 89 (1997) 3104-3112
25. Blair A., and Sutherland H.J. Primitive acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo lack surface expression of c-kit (CD117). Exp. Hematol. 28 (2000) 660-671
26. Jordan C.T., et al. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia 14 (2000) 1777-1784
27. Taussig D.C., et al. Hematopoietic stem cells express multiple myeloid markers: implications for the origin and targeted therapy of acute myeloid leukemia. Blood 106 (2005) 4086-4092
28. - stem cell compartment in acute myeloid leukemia allows to distinguish the malignant from the normal stem cell compartment both at diagnosis and in remission. Leukemia 21 (2007) 1700-1707
29. Pearce D.J., et al. AML engraftment in the NOD/SCID assay reflects the outcome of AML: implications for our understanding of the heterogeneity of AML. Blood 107 (2006) 1166-1173
30. van Rhenen A., et al. High stem cell frequency in acute myeloid leukemia at diagnosis predicts high minimal residual disease and poor survival. Clin. Cancer Res. 11 (2005) 6520-6527
31. Haferlach T., et al. Which compartments are involved in Philadelphia-chromosome positive chronic myeloid leukemia? An answer at the single cell level by combining May-Grünwald-Giemsa staining and fluorescence in situ hybridization techniques. Br. J. Haematol. 97 (1997) 99-106
32. Jamieson C.H.M., et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N. Engl. J. Med. 351 (2004) 657-667
33. Wang J.C.Y., et al. High level engraftment of NOD/SCID mice by primitive normal and leukemic hematopoietic cells from patients with chronic myeloid leukemia in chronic phase. Blood 91 (1998) 2406-2414
34. Eisterer W., et al. Different subsets of primary chronic myeloid leukemia stem cells engraft immunodeficient mice and produce a model of the human disease. Leukemia 19 (2005) 435-441
35. Guzman M.L., et al. Nuclear factor-kappaB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood 98 (2001) 2301-2317
36. Guan Y., et al. Detection, isolation, and stimulation of quiescent primitive leukemic progenitor cells from patients with acute myeloid leukemia (AML). Blood 101 (2003) 3142-3149
37. Terpstra W., et al. Fluorouracil selectively spares acute myeloid leukemia cells with long-term growth abilities in immunodeficient mice and in culture. Blood 88 (1996) 1944-1950
38. Holyoake T., et al. Isolation of a highly quiescent subpopulation of primitive leukemic cells in chronic myeloid leukemia. Blood 94 (1999) 2056-2064
39. Dean M., et al. Tumour stem cells and drug resistance. Nat. Rev. Cancer 5 (2005) 275-284
40. Antonchuk J., et al. HOXB4-induced expansion of adult hematopoietic stem cells ex vivo. Cell 109 (2002) 39-45
41. Thorsteinsdottir U., et al. Overexpression of the myeloid leukemia-associated Hoxa9 gene in bone marrow cells induces stem cell expansion. Blood 99 (2002) 121-129
42. Bhardwaj G., et al. Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation. Nat. Immunol. 2 (2001) 172-180
43. Varnum-Finney B., et al. Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling. Nat. Med. 6 (2000) 1278-1281
44. Reya T., et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423 (2003) 409-414
45. Park I.K., et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 423 (2003) 302-305
46. Lavau C., et al. Immortalization and leukemic transformation of a myelomonocytic precursor by retrovirally transduced HRX-ENL. EMBO J. 16 (1997) 4226-4237
47. Ayton P.M., and Cleary M.L. Molecular mechanisms of leukemogenesis mediated by MLL fusion proteins. Oncogene 20 (2001) 5695-5707
48. Cozzio A., et al. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev. 17 (2003) 3029-3035
49. Akashi K., et al. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404 (2000) 193-197
50. Huntly B.J., et al. MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell 6 (2004) 587-596
51. Lessard J., and Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423 (2003) 255-260
52. Miyamoto T., et al. AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 7521-7526
53. de Guzman C.G., et al. Hematopoietic stem cell expansion and distinct myeloid developmental abnormalities in a murine model of the AML1-ETO translocation. Mol. Cell. Biol. 22 (2002) 5506-5517
54. Li S., et al. The P190, P210, and P230 forms of the BCR/ABL oncogene induce a similar chronic myeloid leukemia-like syndrome in mice but have different lymphoid leukemogenic activity. J. Exp. Med. 189 (1999) 1399-1412
55. + leukemia in mice. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 16870-16875
56. Neering S.J., et al. Leukemia stem cells in a genetically defined murine model of blast crisis CML. Blood 110 (2007) 2578-2585
57. Jaiswal S., et al. Expression of BCR/ABL and BCL2 in myeloid progenitors leads to myeloid leukemias. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 10002-10007
58. Passegue E., et al. JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells. Cell 119 (2004) 431-443
59. Fialkow P.J., et al. Chronic myelocytic leukemia: clonal origin in a stem cell common to the granulocyte, erythrocyte, platelet and monocyte/macrophage. Am. J. Med. 63 (1977) 125-130
60. Coluccia A.M., et al. Bcr-Abl stabilizes beta-catenin in chronic myeloid leukemia through its tyrosine phosphorylation. EMBO J. 26 (2007) 1456-1466
61. Somervaille T.C., and Cleary M.L. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer Cell 10 (2006) 257-268
62. Kelly P.N., et al. Tumor growth need not be driven by rare cancer stem cells. Science 317 (2007) 337
63. Ayton P.M., and Cleary M.L. Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev. 17 (2003) 2298-2307
64. Deshpande A.J., et al. Acute myeloid leukemia is propagated by a leukemic stem cell with lymphoid characteristics in a mouse model of CALM/AF10-positive leukemia. Cancer Cell 10 (2006) 363-374
65. Dash A.B., et al. A murine model of CML blast crisis induced by cooperation between BCR/ABL and NUP98/HOX49. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 7622-7627
66. Druker B.J., et al. Activity of a specific inhibitor of the BCR-ABL tyrosine kinase in the blast crisis of chronic myeloid leukemia and acute lymphoblastic leukemia with the Philadelphia chromosome. N. Engl. J. Med. 344 (2001) 1038-1042
67. Weng A.P., et al. Growth suppression of pre-T acute lymphoblastic leukemia cells by inhibition of notch signaling. Mol. Cell. Biol. 23 (2003) 655-664
68. Guzman M.L., et al. Preferential induction of apoptosis for primary human leukemic stem cells. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 16220-16225
69. Guzman M.L., et al. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood 105 (2005) 4163-4169
70. Xu Q., et al. Survival of acute myeloid leukemia cells requires PI3 kinase activation. Blood 102 (2003) 972-980
71. Xu Q., et al. mTOR regulates cell survival after etoposide treatment in primary AML cells. Blood 106 (2005) 4261-4268
72. Frankfurt O., and Tallman M.S. Strategies for the treatment of acute promyelocytic leukemia. J. Natl. Compr. Canc. Netw. 4 (2006) 37-50
73. Grimwade D., and Enver T. Acute promyelocytic leukemia: where does it stem from?. Leukemia 18 (2004) 375-384
74. Zheng X., et al. Arsenic but not all-trans retinoic acid overcomes the aberrant stem cell capacity of PML/RARα-positive leukemic stem cells. Haematologica 92 (2007) 323-331
75. Bhatia R., et al. Persistence of malignant hematopoietic progenitors in chronic myelogenous leukemia patients in complete cytogenetic remission following imatinib mesylate treatment. Blood 101 (2003) 4701-4707
76. Graham S.M., et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood 99 (2002) 319-325
77. Holtz M.S., et al. Imatinib mesylate (STI571) inhibits growth of primitive malignant progenitors in chronic myelogenous leukemia through reversal of abnormally increased proliferation. Blood 99 (2002) 3792-3800
78. Copland M., et al. Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML but does not eliminate the quiescent fraction. Blood 107 (2006) 4532-4539
79. + CML cells. Blood 109 (2007) 4016-4019
80. Jorgensen H.G., et al. Lonafarnib reduces the resistance of primitive quiescent CML cells to imatinib mesylate in vitro. Leukemia 19 (2005) 1184-1191
81. + progenitors are resistant to apoptosis induced by a wide range of proapoptotic stimuli. Leukemia 19 (2005) 1034-1041
82. Jorgensen H.G., et al. Intermittent exposure of primitive quiescent chronic myeloid leukemia cells to granulocyte-colony stimulating factor in vitro promotes their elimination by imatinib mesylate. Clin. Cancer Res. 12 (2006) 626-633
83. Holtz M., et al. Growth factor stimulation reduces residual quiescent chronic myelogenous leukemia progenitors remaining after imatinib treatment. Cancer Res. 67 (2007) 1113-1120
84. Tsimberidou A.M., et al. The role of gemtuzumab ozogamicin in acute leukaemia therapy. Br. J. Haematol. 132 (2006) 398-409
85. Sperr W.R., et al. CD 33 as a target of therapy in acute myeloid leukemia: current status and future perspectives. Leuk. Lymphoma 46 (2005) 1115-1120
86. Jedema I., et al. Internalization and cell cycle-dependent killing of leukemic cells by Gemtuzumab Ozogamicin: rationale for efficacy in CD33-negative malignancies with endocytic capacity. Leukemia 18 (2004) 316-325
87. Hogge D.E., et al. The efficacy of diphtheria-growth factor fusion proteins is enhanced by co-administration of cytosine arabinoside in an immunodeficient mouse model of human acute myeloid leukemia. Leuk. Res. 28 (2004) 1221-1226
88. Matsunaga T., et al. Interaction between leukemic-cell VLA-4 and stromal fibronectin is a decisive factor for minimal residual disease of acute myelogenous leukemia. Nat. Med. 9 (2003) 1158-1165
89. Bakker A.B., et al. C-type lectin-like molecule-1: a novel myeloid cell surface marker associated with acute myeloid leukemia. Cancer Res. 64 (2004) 8443-8450
90. Ponta H., et al. CD44: from adhesion molecules to signalling regulators. Nat. Rev. Mol. Cell Biol. 4 (2003) 33-45
91. Charrad R.-S., et al. Ligation of the CD44 adhesion molecule reverses blockage of differentiation in human acute myeloid leukemia. Nat. Med. 5 (1999) 669-676
92. Salesse S., and Verfaillie C.M. Mechanisms underlying abnormal trafficking and expansion of malignant progenitors in CML: BCR/ABL-induced defects in integrin function in CML. Oncogene 21 (2002) 8605-8611
93. + leukemia-initiating cells. Blood 106 (2005) 206a
94. Dagia N.M., et al. G-CSF induces E-selectin ligand expression on human myeloid cells. Nat. Med. 12 (2006) 1185-1190
95. + cells present in autologous transplants of chronic myelogenous leukemia (CML) contribute to relapse after autologous bone marrow in CML. Blood 83 (1994) 3068-3076
96. Farmer H., et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434 (2005) 917-921
97. Krampera M., et al. Methodological approach to minimal residual disease detection by flow cytometry in adult B-lineage acute lymphoblastic leukemia. Haematologica 91 (2006) 1109-1112
98. Guinn B.A., et al. Immunotherapy of myeloid leukaemia. Cancer Immunol. Immunother. 56 (2007) 943-957
99. Manz M.G., et al. Prospective isolation of human clonogenic common myeloid progenitors. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 11872-11877